Diverse roles of strigolactone signaling in maize architecture and the uncoupling of a branching-specific subnetwork

Plant Physiology

Volumn 160, Issue 3, 2012, Pages 1303-1317

  Guan, Jiahn Chou ^a   Koch, Karen E ^a   Suzuki, Masaharu ^a   Wu, Shan ^a   Latshaw, Susan ^a   Petruff, Tanya ^a   Goulet, Charles ^a   Klee, Harry J ^a   McCarty, Donald R ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84868333310     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.204503     Document Type: Article

References (70)

1. Aguilar-Martínez JA, Poza-Carrión C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19: 458-472
2. Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, Brewer PB, Beveridge CA, Sieberer T, Sehr EM, Greb T (2011) Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci USA 108: 20242-20247
3. Amusan IO, Rich PJ, Menkir A, Housley T, Ejeta G (2008) Resistance to Striga hermonthica in a maize inbred line derived from Zea diploperennis. New Phytol 178: 157-166
4. Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S (2012) The path from b-carotene to carlactone, a strigolactone-like plant hormone. Science 335: 1348-1351
5. Arite T, Iwata H, Ohshima K, Maekawa M, Nakajima M, Kojima M, Sakakibara H, Kyozuka J (2007) DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J 51: 1019-1029
6. Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, Yamaguchi S, Kyozuka J (2009) d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 50: 1416-1424
7. Auldridge ME, Block A, Vogel JT, Dabney-Smith C, Mila I, Bouzayen M, Magallanes-Lundback M, DellaPenna D, McCarty DR, Klee HJ (2006) Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J 45: 982-993
8. Awad A, Sato D, Kusumoto D, Kamioka H, Takeuchi Y, Yoneyama K (2006) Characterization of strigolactones, germination stimulants for the root parasitic plants Striga and Orobanche, produced by maize, millet and sorghum. Plant Growth Regul 48: 221-227
9. Barker NP, Clark LG, Davis JI, Duvall MR, Guala GF, Hsiao C, Kellogg EA, Linder HP, Mason-Gamer RJ, Mathews SY, et al (2001) Phylogeny and subfamilial classification of the grasses (Poaceae). Ann Mo Bot Gard 88: 373-457
10. Beveridge CA, Dun EA, Rameau C (2009) Pea has its tendrils in branching discoveries spanning a century from auxin to strigolactones. Plant Physiol 151: 985-990
11. Blanc G, Wolfe KH (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16: 1667-1678
12. Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14: 1232-1238
13. Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8: 443-449
14. Braun N, de Saint Germain A, Pillot J-P, Boutet-Mercey S, Dalmais M, Antoniadi I, Li X, Maia-Grondard A, Le Signor C, Bouteiller N, et al (2012) The pea TCP transcription factor PsBRC1 acts downstream of strigolactones to control shoot branching. Plant Physiol 158: 225-238
15. Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA (2009) Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 150: 482-493
16. Chojnacka K, Santoro S, Awartani R, Richards NGJ, Himo F, Aponick A (2011) Synthetic studies on the solanacol ABC ring system by cation-initiated cascade cyclization: implications for strigolactone biosynthesis. Org Biomol Chem 9: 5350-5353
17. Clark RM, Wagler TN, Quijada P, Doebley J (2006) A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nat Genet 38: 594-597
18. Crawford S, Shinohara N, Sieberer T, Williamson L, George G, Hepworth J, Müller D, Domagalska MA, Leyser O (2010) Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 137: 2905-2913
19. de Alencar Figueiredo LF, Calatayud C, Dupuits C, Billot C, Rami JF, Brunel D, Perrier X, Courtois B, Deu M, Glaszmann JC (2008) Phylogeographic evidence of crop neodiversity in sorghum. Genetics 179: 997-1008
20. Delaux PM, Xie X, Timme RE, Puech-Pages V, Dunand C, Lecompte E, Delwiche CF, Yoneyama K, Bécard G, Séjalon-Delmas N (2012) Origin of strigolactones in the green lineage. New Phytol 195: 857-871
21. Desfeux C, Clough SJ, Bent AF (2000) Female reproductive tissues are the primary target of Agrobacterium-mediated transformation by the Arabidopsis floral-dip method. Plant Physiol 123: 895-904
22. Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386: 485-488
23. Doust AN (2007) Architectural evolution and its implications for domestication in grasses. Ann Bot (Lond) 100: 941-950
24. Doust AN, Devos KM, Gadberry MD, Gale MD, Kellogg EA (2004) Genetic control of branching in foxtail millet. Proc Natl Acad Sci USA 101: 9045-9050
25. Drummond RSM, Martínez-Sánchez NM, Janssen BJ, Templeton KR, Simons JL, Quinn BD, Karunairetnam S, Snowden KC (2009) Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE7 is involved in the production of negative and positive branching signals in petunia. Plant Physiol 151: 1867-1877
26. Dun EA, de Saint Germain A, Rameau C, Beveridge CA (2012) Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiol 158: 487-498
27. Finlayson SA (2007) Arabidopsis Teosinte Branched1-like 1 regulates axillary bud outgrowth and is homologous to monocot Teosinte Branched1. Plant Cell Physiol 48: 667-677
28. Finlayson SA, Krishnareddy SR, Kebrom TH, Casal JJ (2010) Phytochrome regulation of branching in Arabidopsis. Plant Physiol 152: 1914-1927
29. Foo E, Bullier E, Goussot M, Foucher F, Rameau C, Beveridge CA (2005) The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. Plant Cell 17: 464-474
30. Gao Z, Qian Q, Liu X, YanM, Feng Q, Dong G, Liu J, Han B (2009) Dwarf 88, a novel putative esterase gene affecting architecture of rice plant. Plant Mol Biol 71: 265-276
31. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, Letisse F, Matusova R, et al (2008) Strigolactone inhibition of shoot branching. Nature 455: 180-194
32. Gomez-Roldan V, Roux C, Girard D, Bécard G, Puech-Pagés V (2007) Strigolactones: promising plant signals. Plant Signal Behav 2: 163-164
33. Goulet C, Klee HJ (2010) Climbing the branches of the strigolactones pathway one discovery at a time. Plant Physiol 154: 493-496
34. Hayward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151: 400-412
35. Hu Z, Yan H, Yang J, Yamaguchi S, Maekawa M, Takamure I, Tsutsumi N, Kyozuka J, Nakazono M (2010) Strigolactones negatively regulate mesocotyl elongation in rice during germination and growth in darkness. Plant Cell Physiol 51: 1136-1142
36. Hubbard L, McSteen P, Doebley J, Hake S (2002) Expression patterns and mutant phenotype of teosinte branched1 correlate with growth suppression in maize and teosinte. Genetics 162: 1927-1935
37. Knöller AS, Blakeslee JJ, Richards EL, Peer WA, Murphy AS (2010) Brachytic2/ZmABCB1 functions in IAA export from intercalary meristems. J Exp Bot 61: 3689-3696
38. Koltai H (2011) Strigolactones are regulators of root development. New Phytol 190: 545-549
39. Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483: 341-344
40. Ledger SE, Janssen BJ, Karunairetnam S, Wang T, Snowden KC (2010) Modified CAROTENOID CLEAVAGE DIOXYGENASE8 expression correlates with altered branching in kiwifruit (Actinidia chinensis). New Phytol 188: 803-813
41. Lin H, Wang R, Qian Q, Yan M, Meng X, Fu Z, Yan C, Jiang B, Su Z, Li J, Wang Y (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21: 1512-1525
42. Liu W, Wu C, Fu Y, Hu G, Si H, Zhu L, Luan W, He Z, Sun Z (2009) Identification and characterization of HTD2: a novel gene negatively regulating tiller bud outgrowth in rice. Planta 230: 649-658
43. Mashiguchi K, Sasaki E, Shimada Y, Nagae M, Ueno K, Nakano T, Yoneyama K, Suzuki Y, Asami T (2009) Feedback-regulation of strigolactone biosynthetic genes and strigolactone-regulated genes in Arabidopsis. Biosci Biotechnol Biochem 73: 2460-2465
44. Matusova R, Rani K, Verstappen FW, Franssen MCR, Beale MH, Bouwmeester HJ (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139: 920-934
45. Messing SAJ, Gabelli SB, Echeverria I, Vogel JT, Guan JC, Tan BC, Klee HJ, McCarty DR, Amzel LM (2010) Structural insights into maize viviparous14, a key enzyme in the biosynthesis of the phytohormone abscisic acid. Plant Cell 22: 2970-2980
46. Minakuchi K, Kameoka H, Yasuno N, Umehara M, Luo L, Kobayashi K, Hanada A, Ueno K, Asami T, Yamaguchi S, Kyozuka J (2010) FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant Cell Physiol 51: 1127-1135
47. Motta A, Basso B, Dell'Orto M, Briat J-F, Soave C (2001) Ferritin synthesis in response to iron in the Fe-inefficient maize mutant ys3. Plant Physiol Biochem 39: 461-465
48. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: 2002-2007
49. Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, Yoneyama K, Nogué F, Rameau C (2011) Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138: 1531-1539
50. Rasmussen A, Mason MG, De Cuyper C, Brewer PB, Herold S, Agusti J, Geelen D, Greb T, Goormachtig S, Beeckman T, Beveridge CA (2012) Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol 158: 1976-1987
51. Remigereau MS, Lakis G, Rekima S, Leveugle M, Fontaine MC, Langin T, Sarr A, Robert T (2011) Cereal domestication and evolution of branching: evidence for soft selection in the Tb1 orthologue of pearl millet (Pennisetum glaucum [L.] R. Br.). PLoS ONE 6: e22404
52. Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N, Cardoso C, Lopez-Raez JA, Matusova R, Bours R, Verstappen F, Bouwmeester H (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155: 721-734
53. Settles AM, Latshaw S, McCarty DR (2004) Molecular analysis of highcopy insertion sites in maize. Nucleic Acids Res 32: e54
54. Shen H, Luong P, Huq E (2007) The F-box protein MAX2 functions as a positive regulator of photomorphogenesis in Arabidopsis. Plant Physiol 145: 1471-1483
55. Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, Simons JL, Karunairetnam S, Gleave AP, Clark DG, Klee HJ (2005) The Decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17: 746-759
56. Sorefan K, Booker J, Haurogné K, Goussot M, Bainbridge K, Foo E, Chatfield S, Ward S, Beveridge C, Rameau C, Leyser O (2003) MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev 17: 1469-1474
57. Stirnberg P, van De Sande K, Leyser HM (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129: 1131-1141
58. Studer A, Zhao Q, Ross-Ibarra J, Doebley J (2011) Identification of a functional transposon insertion in the maize domestication gene tb1. Nat Genet 43: 1160-1163
59. Tsuchiya Y, Vidaurre D, Toh S, Hanada A, Nambara E, Kamiya Y, Yamaguchi S, McCourt P (2010) A small-molecule screen identifies new functions for the plant hormone strigolactone. Nat Chem Biol 6: 741-749
60. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-200
61. Vielle-Calzada JP, Martínez de la Vega O, Hernández-Guzmán G, Ibarra-Laclette E, Alvarez-Mejía C, Vega-Arreguín JC, Jiménez-Moraila B, Fernández-Cortés A, Corona-Armenta G, Herrera-Estrella L, et al (2009) The Palomero genome suggests metal effects on domestication. Science 326: 1078
62. Vogel JT, Walter MH, Giavalisco P, Lytovchenko A, Kohlen W, Charnikhova T, Simkin AJ, Goulet C, Strack D, Bouwmeester HJ, et al (2010) SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J 61: 300-311
63. Vollbrecht E, Duvick J, Schares JP, Ahern KR, Deewatthanawong P, Xu L, Conrad LJ, Kikuchi K, Kubinec TA, Hall BD, et al (2010) Genome-wide distribution of transposed Dissociation elements in maize. Plant Cell 22: 1667-1685
64. Wang Y, Li J (2011) Branching in rice. Curr Opin Plant Biol 14: 94-99
65. Waters MT, Brewer PB, Bussell JD, Smith SM, Beveridge CA (2012a) The Arabidopsis ortholog of rice DWARF27 acts upstreamofMAX1 in the control of plant development by strigolactones. Plant Physiol 159: 1073-1085
66. Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, Smith SM (2012b) Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 139: 1285-1295
67. Whipple CJ, Kebrom TH, Weber AL, Yang F, Hall D, Meeley R, Schmidt R, Doebley J, Brutnell TP, Jackson DP (2011) grassy tillers1 promotes apical dominance in maize and responds to shade signals in the grasses. Proc Natl Acad Sci USA 108: E506-E512
68. Xie X, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48: 93-117
69. Zhou L, Zhang J, Yan J, Song R (2011) Two transposable element insertions are causative mutations for the major domestication gene teosinte branched 1 in modern maize. Cell Res 21: 1267-1270
70. Zou J, Zhang S, Zhang W, Li G, Chen Z, Zhai W, Zhao X, Pan X, Xie Q, Zhu L (2006) The rice HIGH-TILLERING DWARF1 encoding an ortholog of Arabidopsis MAX3 is required for negative regulation of the outgrowth of axillary buds. Plant J 48: 687-698